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PET/CT variants and pitfalls in malignant melanoma
Cancer Imaging volume 22, Article number: 3 (2022)
18F-FDG PET/CT plays an increasingly pivotal role in the staging and post-treatment monitoring of high-risk melanoma patients, augmented by the introduction of therapies, including tyrosine kinase inhibitors (TKI) and immune checkpoint inhibitors (ICIs), that have novel modes of action that challenge conventional response assessment. Simultaneously, technological advances have been regularly released, including advanced reconstruction algorithms, digital PET and motion correction, which have allowed the PET community to detect ever-smaller cancer lesions, improving diagnostic performance in the context of indications previously viewed as limitations, such as detection of in-transit disease and confirmation of the nature of small pulmonary metastases apparent on CT.
This review will provide advice regarding melanoma-related PET protocols and will focus on variants encountered during the imaging of melanoma patients. Emphasis will be made on pitfalls related to non-malignant diseases and treatment-related findings that may confound accurate interpretation unless recognized. The latter include signs of immune activation and immune-related adverse events (irAEs). Technology-related pitfalls are also discussed, since while new PET technologies improve detection of small lesions, these may also induce false-positive cases and require a learning curve to be observed. In these times of the COVID 19 pandemic, cases illustrating lessons learned from COVID 19 or vaccination-related pitfalls will also be described.
Epidemiological studies report a rapid increase in the incidence of melanoma over the past 50 years or so, primarily in Caucasians, despite some slowing of the rate of increase around 1990–2000, probably reflecting increased awareness of the risk of excessive sun exposure and consequent UV damage to DNA. Unlike other solid tumors, melanoma mostly affects young and middle-aged people. The median age at the time of diagnosis of melanoma is 57 years . However, in Australia, which has one of the highest incidences of melanoma in the world, the rate of new diagnoses increases with age, particularly in males. Close to 80% of cases present with early-stage disease (https://ncci.canceraustralia.gov.au/diagnosis/distribution-cancer-stage/distribution-cancer-stage) and have high survival rates. High-risk melanoma represents a major burden on society through both direct costs and loss of productivity.
Mucosal/cutaneous vs uveal melanoma
Less than 5% of all primary melanomas arise from sites other than the skin. These include mucosal surfaces, meninges and the choroidal layer of the eye, which have a common ectodermal origin . Mucosal melanomas can arise in the nasopharynx, larynx, tracheobronchial tracts, esophagus, anorectal and genitourinary tracts. Approximately 50% affect the head and neck region with a predominance in the sinuses and nasal cavities . Mucosal melanomas are considered to be more aggressive than their cutaneous counterparts, possibly linked to delayed diagnosis with larger tumor masses, and metastatic extension at diagnosis (30%).
Uveal melanoma is a distinct clinico-pathological entity, differing in many aspects from cutaneous melanoma, including a distinct set of associated mutations [4, 5]. Its clinical course is unpredictable and metastatic disease can develop after a long disease-free interval.
Approximately 3% of metastatic melanomas are of unknown primary . This potentially reflects spontaneous regression of the primary as a result of innate immune responses.
Pattern of spread of melanoma
The main cause of death in melanoma patients is widespread metastasis. Metastases develop in regional lymph nodes, as satellite or in-transit lesions, or in distant organs. In-transit metastases occur in 5 to 8% of patients with high-risk melanoma of the limb and can present as single or multiple (sub) cutaneous nodules close to the primary tumour (satellitosis if < 3 cm from the primary tumour) or scattered over the whole extremity . They can appear synchronously together with the primary tumour or as a regional relapse, and frequently precede the appearance of systemic metastases . Prolonged survival can occur following locoregional therapies .
When it comes to distant metastases, autopsy cases have shown that multiple organ metastases were present in 95% of the patients, the most common organs involved being lymph nodes (73.6%), lungs (71.3%), liver (58.3%), brain (49.1%), bone (48.6%), heart (47.2%), adrenal glands (46.8%), and gastrointestinal tract (43.5%) . A varying percentage (14%  to 67% ) of patients presenting with single organ metastasis at the time of tumor relapse has been reported in large series of patients referred to surgery, though these figures were reported at a time when modern PET sytems were not routinely used for staging and restaging of melanoma patients.
Rather than spreading to regional nodes, uveal melanoma metastasizes haematogenously, predominantly to the liver [13, 14]. Metastases to the liver develop within 15 years after the initial diagnosis and treatment in approximately 50% of patients with posterior uveal melanoma [4, 5].
18F-FDG PET/CT has been proven to have high diagnostic performance for the detection of soft-tissue, nodal and visceral metastases at initial staging or during follow-up  and is able to identify tumor response early in the course of TKI treatment . In the framework of immunotherapy, 18F-FDG PET/CT has the unparalleled capability of assessing tumor response on a whole-body basis and detecting signs of immune activation as well as immune-related adverse effects (irAEs) [17,18,19,20,21,22].
In addition to the usual compliance with PET tumour imaging guidelines and harmonizing standards , several points regarding the PET acquisition protocol need to be raised. First, while including the brain in the field of view is not routine at many PET centres, the skull base should be included, at least for therapy assessment examinations, so that immune-related hypophysitis can be detected. While MRI is the preferred method for assessing brain and leptomeningeal metastases from melanoma, the high metabolic activity of melanoma, particularly when accompanied by surrounding vasogenic oedema can make intracranial involvement readily apparent on PET and given the small incremental imaging time to acquire from the vertex of the skull, this is recommended by the authors. When the arms are elevated to improve imaging of the thorax and axillae, more of the upper limbs are also included when whole-brain imaging is acquired.
Second, accurate staging or restaging of patients with melanoma of the extremities requires a whole-body acquisition in the case of primary tumour located on the lower limbs and the arms along the body for primary tumours located on the upper limbs. Indeed, digital PET using small-voxel reconstructions  or modern reconstruction algorithms  brings an additional value for the detection of in-transit metastases in melanoma patients, by reducing the number of indeterminate findings and minimizing falsely negative scans compared to earlier PET systems. It is noteworthy that for overweight patients, hands should be positioned on the pelvis to avoid any truncation artefact of the arms at the edges of the field of view .
If myocardial metastases are suspected, a special diet, long fasting period and heparin can be used to suppress physiological myocardial 18F-FDG uptake .
PET reports for therapy monitoring of patients receiving immune checkpoint inhibitors (ICIs) should include therapy response according to validated criteria, presence of signs of immune activation and signs of toxicity, especially immune-related adverse events (irAEs) requiring withdrawal of ICIs and/or corticosteroids, e.g., colitis and pneumonitis. Proposals for structured PET report can be found elsewhere [17, 28, 29].
Pitfalls related to non-malignant diseases
Acne and furunculosis
Benign uptake related to acne and cutaneous infectious processes should not be mistaken for subcutaneous or in-transit metastases. While acne lesions tend to occur on the trunk and face, as shown in Fig. 1. Quick clinical examination before discharging the patient from the PET unit will avoid false-positive reports in the case of evident infectious skin disorders, while more complex situations may require skin examination by a dermatologist.
The PET reader should be aware of potential technology-related pitfalls, as new PET technologies, such as advanced reconstruction algorithms and digital PET using small-voxel reconstruction, have improved detection of small lesions , but may also induce false-positive cases by significantly increasing apparent uptake in benign lesions (Figs. 2 and 3).
Post vaccine nodal uptake
PET centers scanning cancer patients after the introduction of the COVID 19 vaccination program have witnessed moderate to intense local or systemic inflammatory responses in some patients . It is noteworthy that such local nodal inflammatory responses have already been observed in patients having received Influenza vaccines , but the frequency of these observations with COVID19 vaccine and the presence of multiple nodal uptake at higher echelon nodal stations is unprecedented.
While some of them may be pretty obvious, appearing as subcutaneous and/or muscular uptake at the site of injection and contiguous nodal uptake, some other situations may be misleading for tumour uptake, especially in patients staged or followed-up for melanoma of the upper limbs. Concerning nodal uptake, it is noteworthy that foci may vary in intensity and can co-exist with both benign CT patterns (oblong shape, fatty hilum) and suspicious round shape may occur, as shown in Fig. 4. Also misleading can be the presence of benign nodal uptake in secondary echelon nodes. These lymph nodes may remain 18F-FDG -avid up to 10 weeks or later after vaccination . For these reasons, it is prudent to adapt PET scheduling not only within treatment constraints but also accommodate the vaccination scheme of melanoma patients, as suggested recently in the largest series of vaccination-related inflammatory changes reported in the Israeli population .
Sarcoid-like granuloma, especially mediastinal but sometimes systemic sarcoid
Both at diagnosis and during therapy of melanoma, granulomatous disease involving nodes and other organs may cause diagnostic difficulties. Although the typical distribution of sarcoid-like lymphadenopathy includes symmetrical, generally non-enlarged hilar and mediastinal nodes with increased uptake, atypical patterns can occur. Peri-portal nodes and focal splenic lesions are not uncommon. The evolution of the sarcoid-like granulomatous disease in response to immune checkpoint therapy is highly variable and can persist beyond the withdrawal of ICIs and fluctuate in activity over time (Fig. 5).
Technology-related pitfalls: characterization of pulmonary nodules
Due to respiratory movement, the 18F-FDG uptake and CT characteristics of the pulmonary nodules in the base of lungs may be subject to partial volume effect (Fig. 6). In these cases, a dedicated fine slice CT of the chest in full inspiration may further characterize the suspected findings. Upon detection of pulmonary nodules, other differential diagnosis needs to be considered including benign and neoplastic process and ultimately a histopathologic confirmation may be needed.
It is expected in the near future that advancements in PET motion correction will allow to better characterize small nodules located in the base of the lungs. Specifically, data-driven motion correction and the emergence of artificial intelligence tools are opening new opportunities for motion handling in clinical PET .
Variants: false-negative or very low uptake in liver metastases from choroidal melanoma
Uveal melanoma metastasizes haematogenously, predominantly to the liver and metastases may be of small volume. Attention should be paid to doubtful 18F-FDG foci, as small volume liver metastases may occur, and uptake intensity may be lower than that observed in other histological subtypes of melanoma. This is more problematic in overweight or obese patients in whom statistical considerations lead to greater inhomogeneity of apparent 18F-FDG uptake (as shown in Figs. 7 and 8 below), indeterminate 18F-FDG foci should lead to follow-up PET or additional radiological exploration. It is expected that technological evolutions such as digital PET with small-voxel reconstruction and/or enhancement of images with the convolutional neural network will further improve image quality in the liver and detection of small volume metastatic disease . Because of the para-magnetic properties of melanin, MRI is a relatively sensitive technique for the detection of uveal melanoma metastases to liver and should be recommended in the setting of clinical suspicion or equivocal PET/CT findings.
Pitfalls related to treatment
Frequently encountered patterns
Colitis may be a life-threatening irAE, requiring withdrawal of ICI and/or treatment with corticosteroids. It is noteworthy that colitis often presents as intense circumferential uptake without wall thickening and/or fat stranding on CT, and should therefore not be confused with benign uptake due to metformin treatment in diabetic patients.
A typical feature of immune-related colitis is prominent of the haustra as well giving rise to an appearance similar to a “string of pearls”. Unlike physiological bowel activity, which is often segmental, the entire colon is generally involved by autoimmune colitis. It should be noted that immune-related adverse events can occur simultaneously or be temporally unrelated (Fig. 9).
Diffuse enteritis masking small bowel and serosal metastases
Small bowel is a common site for gastrointestinal metastasis in melanoma, however, the history and clinical findings are nonspecific and may mimic immune-related gastritis and enteritis. The presence of the latter, could potentially mask small bowel metastases on 18F-FDG PET/CT (Fig. 10).
Along with colitis, pneumonitis (Fig. 11) may be a life-threatening irAE, requiring withdrawal of ICI and/or treatment with corticosteroids.
Although immune-related pneumonitis is the most common cause of patchy increased 18F-FDG uptake in the lung, other pathologies should always be considered. In the COVID-19 era, these include pulmonary manifestations of viral infection . Pulmonary sarcoidosis is also a differential diagnosis but is more often nodular than of a ground-glass or diffuse subpleural distribution. Of course, both conditions may co-exist.
Autoimmune hepatitis is relatively common as a side effect of ICI therapy but is usually detected on routine biochemistry surveillance. Occasionally it can persist and be apparent on 18F-FDG PET/CT (Fig. 12).
Unusual irAEs during immunotherapy
Pancreatitis mimicking malignancy
Pancreatitis has been reported to occur in 2.7% of patients receiving ICIs, more frequently with anti-CTLA4 (3.08% versus 0.94% for anti PD1) . Also, melanoma patients treated with ICIs have increased incidence of pancreatitis as compared to other solid tumours. Although not misleading when appearing as homogeneous increased 18F-FDG uptake involving the whole gland, pancreatitis can also appear as focal uptake mimicking either primary tumour or metastatic disease (Fig. 13).
Peripheral vasculitis (Fig. 14).
Fasciitis (Fig. 15).
TKI-induced Hemophagocytic lymphohistiocytosis (HLH): Not to be confused with a “banal” inversion of the liver to spleen ratio
HLH is related to an excessive immune activation leading to high fever, cytopenia, hepatosplenomegaly and multi-organ injury. HLH has been reported to induce an increased splenic uptake on 18F-FDG PET/CT greater than that observed during sepsis . HLH can be observed during treatment with BRAF/MEK inhibitors, as shown in the case below (Fig. 16), and has also been reported in patients receiving ICIs.
Severe autoimmune skin involvement is an uncommon but recognized complication of ICI. Bullous pemphigoid is the most common of these (Fig. 17).
Multiorgan irAEs including nephritis
Autoimmune renal pathologies are rare but important irAEs related to ICI treatment and normally diagnosed by routine laboratory testing but occasionally apparent on 18F-FDG PET/CT. Typical features are renal enlargement with increased renal parenchymal retention of tracer (Fig. 18).
Conclusion and perspectives
Technological improvements allow us to revisit clinical problems previously viewed as limitations of PET such as detection of in-transit disease, evaluation of small pulmonary nodules apparent on CT and detection of liver metastases in choroidal melanoma, but sometimes produce artefacts and pitfalls requiring a learning curve to be observed.
Knowledge of variants and treatment-related pitfalls is crucial to avoid misinterpretation. ICIs-related pitfalls should not be regarded as a drawback of PET imaging, as they actually reflect the unique capability of PET to perform whole-body imaging and capture signs of immune activation in addition to performing therapy monitoring.
In these times of COVID 19 pandemic, PET scheduling should probably be adapted not only within treatment constraints but also accommodate the vaccination scheme of melanoma patients to avoid false-positive results. Despite this, tricky situations may occur, such as differentiating active COVID-19 related lung involvement from immune-pneumonitis. In any case, PET reporting should be made with knowledge of clinical findings (if needed quick physical examination in the PET unit may be required), laboratory and correlative morphological imaging, and obviously, collaboration with the referring physician and discussion at tumour boards remains crucial for an efficient patient’s management.
Availability of data and materials
tyrosine kinase inhibitors
immune checkpoint inhibitors
- irAEs :
immune-related adverse events
positron emission tomography
- 18F-FDG :
magnetic resonance imaging
maximum intensity projection
European association of nuclear medicine research limited
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The authors are grateful to the staff members of their PET units (secretaries, technologists, Radiopharmacists and Medical Physicists) and colleagues from tumour boards for fruitful discussions around the difficults cases presented in this review.
Ethics approval and consent to participate
cases from the Peter MacCallum Cancer Centre Ethics Committee approval number 17/231R. Due to retrospective nature of the study and no intervention the consent from the individuals were waived. Cases from the Caen University Hospital: French observational studies without any additional therapy or monitoring procedure do not need the approval of an ethics committee. Notheless, in accordance with the European General Data Protection Regulation, we sought approval to collect data for this work from the national committee for data privacy, with the registration no. 2081250 v 0.
Consent for publication
Cases from the Peter MacCallum Cancer Centre: waived or covered by pre-existing consent provided within various clinical trials in which individual patients were enrolled. Cases from the Caen University Hospital: all patients refered to the PET unit receive written information for the use of anonymised images from their examinations for teaching and research purposes and may opt out.
Professor Hicks is the Co-Editor-in-Chief of Cancer Imaging but had no role in assigning reviewers or any other aspect of the review process. For other authors there are none to disclose.
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Aide, N., Iravani, A., Prigent, K. et al. PET/CT variants and pitfalls in malignant melanoma. Cancer Imaging 22, 3 (2022). https://doi.org/10.1186/s40644-021-00440-4
- Pitfalls, variants
- PET technology